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The Expression Profiles of Mrnas and Lncrnas in Buffalo Muscle Stem Cells Driving Myogenic Differentiation

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The Expression Profiles of Mrnas and Lncrnas in Buffalo Muscle Stem Cells Driving Myogenic Differentiation ORIGINAL RESEARCH published: 07 July 2021 doi: 10.3389/fgene.2021.643497 The Expression Profiles of mRNAs and lncRNAs in Buffalo Muscle Stem Cells Driving Myogenic Differentiation Ruimen Zhang 1†, Jinling Wang 1†, Zhengzhong Xiao 2†, Chaoxia Zou 1, Qiang An 1, Hui Li 1, Xiaoqing Zhou 2, Zhuyue Wu 2, Deshun Shi 1, Yanfei Deng 1*, Sufang Yang 1,3* and Yingming Wei 1* 1 State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Animal Reproduction Institute, Guangxi University, Nanning, China, 2 The Animal Husbandry Research Institute of Guangxi Autonomous, Nanning, China, 3 International Zhuang Medical Hospital Affiliated to Guangxi University Chinese Medicine, Nanning, China Edited by: Guohua Hua, Huazhong Agricultural Buffalo breeding has become an important branch of the beef cattle industry. Hence, it University, China is of great significance to study buffalo meat production and meat quality. However, the Reviewed by: expression profiles of mRNA and long non-coding RNAs (lncRNA) molecules in muscle Ikhide G. Imumorin, stem cells (MuSCs) development in buffalo have not been explored fully. We, therefore, Georgia Institute of Technology, United States performed mRNA and lncRNA expression profiling analysis during the proliferation Bo Wang, and differentiation phases of MuSCs in buffalo. The results showed that there were China Agricultural University, China 4,820 differentially expressed genes as well as 12,227 mRNAs and 1,352 lncRNAs. *Correspondence: Yanfei Deng These genes were shown to be enriched in essential biological processes such as [email protected] cell cycle, p53 signaling pathway, RNA transport and calcium signaling pathway. We Sufang Yang also identified a number of functionally important genes, such as MCMC4, SERDINE1, [email protected] Yingming Wei ISLR, LOC102394806, and LOC102403551, and found that interference with MYLPF [email protected] expression significantly inhibited the differentiation of MuSCs. In conclusion, our research †These authors have contributed revealed the characteristics of mRNA and lncRNA expression during the differentiation of equally to this work buffalo MuSCs. This study can be used as an important reference for the study of RNA regulation during muscle development in buffalo. Specialty section: This article was submitted to Keywords: buffalo, muscle stem cells, mRNAs, non-coding RNAs, myogenesis Livestock Genomics, a section of the journal Frontiers in Genetics INTRODUCTION Received: 18 December 2020 Accepted: 25 May 2021 There is an annual increase in the global consumption of beef and it is an indispensable food in our Published: 07 July 2021 modern society, and therefore the beef cattle industry occupies an increasingly important position Citation: in modern agricultural practices (Bonny et al., 2015). According to statistics, in 2019, China’s beef Zhang R, Wang J, Xiao Z, Zou C, production was 6.85 million tons and beef imports were 1.66 million tons with a year-on-year An Q, Li H, Zhou X, Wu Z, Shi D, increase of approximately 57%. It is anticipated that China’s future beef demand will continue to Deng Y, Yang S and Wei Y (2021) The rise. Therefore, China urgently needs a viable and thriving beef cattle industry in order to provide its Expression Profiles of mRNAs and lncRNAs in Buffalo Muscle Stem Cells society with larger amounts of high-quality beef (Mwangi et al., 2019; Ornaghi et al., 2020). There is Driving Myogenic Differentiation. a need for us to conduct research on the growth and meat quality of locally produced beef as well as Front. Genet. 12:643497. to explore the potential molecular information of breeding stocks so as to provide reference values doi: 10.3389/fgene.2021.643497 for future breeding protocols (Grigoletto et al., 2020). Frontiers in Genetics | www.frontiersin.org 1 July 2021 | Volume 12 | Article 643497 Zhang et al. Buffalo Differentiated MuSCs Expression Profiles In ruminants, skeletal muscle tissue accounts for about 40– meat production. This culminated in the successful construction 60% of the adult animal body weight, which not only determines of the buffalo genomic DNA sequence map (Low et al., 2019). the level of meat production performance, but also has an Recently our laboratory analyzed the regulatory networks of important impact on meat quality. There is a group of myoblasts- lncRNA-mRNA interactions in the muscle tissue of cattle and muscle stem cells (MuSCs), which are the source of skeletal buffalo (Li et al., 2020). muscle formation and regeneration, and these have the potential However, when compared to cattle, buffalo muscle has the for differentiation and proliferation of muscle-derived stem cells characteristics of possessing greater shear force and consisting (Feige and Rudnicki, 2018; Feige et al., 2018). This is also the of thicker muscle fibers. At present, the molecular mechanisms current cell model for studying skeletal muscle development. that regulate buffalo muscle fibers formation are still unclear Under certain conditions, these cells can be activated causing the (Huang et al., 2021). We hypothesized that there are key MuSCs proliferate and differentiate. signaling pathway(s) which control the myogenic differentiation One of the main challenges in the field of muscle research is to of MuSCs. We, therefore, analyzed the mRNA expression understand how the genes that are involved in specialized muscle of MuSCs before and after myogenic differentiation through functions at the transcriptional and post-transcriptional levels transcriptome sequencing strategies in an attempt to screen the are regulated. Undoubtedly, myogenic regulatory factors (MRFs) signal pathways that may regulate muscle fiber development. (Hernandez-Hernandez et al., 2017), myocyte enhancer factor- Other recent studies have also shown that differential expression 2 (MEF2) (Taylor and Hughes, 2017), and PAX3/PAX7 genes lncRNAs also play an important physiological function during are the main genes involved in the growth and development of cellular differentiation of MuSCs (Zhu et al., 2017). This study skeletal muscle. Initially, long non-coding RNAs (lncRNAs) were further expands the understanding of skeletal muscle biology, considered to be transcriptional noise but later studies showed and provides a reference target for the genetic improvement of these RNAs play an important function in many biological buffalo and the production and cultivation of meat in vitro and processes (Jae and Dimmeler, 2020). Epigenetic control and in vivo. transcriptional regulation, translation, RNA metabolism, stem cell maintenance and differentiation, autophagy and apoptosis, embryonic development, and other aspects have also been shown MATERIALS AND METHODS to play important roles (Chen et al., 2020). With the discovery of a large number of important muscle regulators such as MuSCs Culture and Differentiation lncRNA H19 (Xu et al., 2017), Neat1 (Wang et al., 2019), lnc- All experiments regarding animals were performed in the State 133b (Jin et al., 2017), circLOM7 (Wei et al., 2017), more and Key Laboratory for Conservation and Utilization of Subtropical more ncRNAs related to muscle development have also been Agro-bio-resources, and were conducted in accordance with its widely characterized (Martone et al., 2019). At the same time, guidelines for the care and use of laboratory animals. Primary the important role of related coding RNAs, lncRNAs, and other water buffalo MuSCs were isolated and cultured from fetal- molecules in the development of skeletal muscle in agricultural derived longissimus muscle as described in Supplementary File animals are gradually being explored. 1, using a combination digestion method of type I collagenase So far, with the emergence of RNA structure detection and trypsin. MuSCs were cultured in high-glucose DMEM technologies such as Frag-seq (Underwood et al., 2010), supplemented with fetal bovine serum (Hyclone, USA; 10% FBS and 20% FBS, respectively) and antibiotics [1% penicillin and (ss/dsRNA)-seq, and SHAPE-seq, have allowed scientists to ◦ characterize the structure of RNAs obtained from different streptomycin; growth medium (GM)] at 5% CO2, 37 C. To tissues and cell components. When these data were combined induce MuSCs myogenic differentiation, MuSCs were switched with knowledge of RNA transformation events, such as miRNA to a differentiation medium (DMEM, 2% horse serum; DM) targeting, RNA modification, and the function of RNA binding when cells were almost 90% confluent for up to 4 days. proteins (RPBs), they have emphasized the importance of RNA structure during gene regulation (Li et al., 2012). Moreover, most Sample Preparation of these studies are focused on mRNAs and ncRNAs in order to The tissues from Chinese buffalo at embryonic stage (90 days) explore the biological functions of RNA structure. were collected at a local slaughterhouse in Nanning, Guangxi As a characteristic species of southern China, the potential use province. Tissue samples, including muscle, liver, heart, lung, of the buffalo as a meat source has gradually attracted attention. skin, kidney, brain, stomach, and intestine, were collected and The buffalo breeding industry has become a food basket project immediately frozen in liquid nitrogen. Proliferation of MuSCs for urban residents, but the meat production and meat quality of was labeled as the GM samples (n = 3) and differentiation of these buffalo needs to be improved for it to be an acceptable alternative was then called the DM samples (n = 3). The samples were kept to cattle (Li et al., 2020). Previously,
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